Molecular characterization of human-pathogenic microsporidia and cyclospora cayetanensis isolated from various water sources in Spain: A year-long longitudinal study

Applied and Environmental Microbiology

Volumn 79, Issue 2, 2013, Pages 449-459

  Galván, Ana Luz ^a,b   Magnet, Angela ^a   Izquierdo, Fernando ^a   Fenoy, Soledad ^a   Rueda, Cristina ^a   adillo, Carmen Fernández V ^a   Henriques Gil, Nuno ^a   del Aguila, Carmen ^a  

^a UNIVERSIDAD SAN PABLO CEU   (Spain)

^b UNIVERSIDAD DE ANTIOQUIA   (Colombia)

Author keywords

[No Author keywords available]

Indexed keywords

ENCEPHALITOZOON CUNICULI; ENCEPHALITOZOON INTESTINALIS; LONGITUDINAL STUDY; MADRID , SPAIN; MICROSPORIDIA; MOLECULAR CHARACTERIZATION; RECREATIONAL WATER; RIVER BASINS; WASTEWATER TREATMENT PLANTS; WATER SAMPLES; WATER SOURCE;

BIOTECHNOLOGY; MICROBIOLOGY;

PROTOZOA;

WATER;

BACTERIUM; DRINKING WATER; EPIDEMIOLOGY; GENOTYPE; HEALTH RISK; HOST-PATHOGEN INTERACTION; MOLECULAR ANALYSIS; PATHOGENICITY; RIVER BASIN; WASTEWATER; WATER TREATMENT;

ARTICLE; CLASSIFICATION; CYCLOSPORA; GENETIC VARIABILITY; GENETICS; GENOTYPE; HUMAN; ISOLATION AND PURIFICATION; LONGITUDINAL STUDY; MICROBIOLOGY; MICROSPORIDIA; PARASITOLOGY; POLYMERASE CHAIN REACTION; SPAIN;

CYCLOSPORA; GENETIC VARIATION; GENOTYPE; HUMANS; LONGITUDINAL STUDIES; MICROSPORIDIA; POLYMERASE CHAIN REACTION; SPAIN; WATER; WATER MICROBIOLOGY;

MADRID [SPAIN]; SPAIN;

ANNCALIIA; CYCLOSPORA; CYCLOSPORA CAYETANENSIS; ENCEPHALITOZOON CUNICULI; ENCEPHALITOZOON INTESTINALIS; ENTEROCYTOZOON BIENEUSI; MICROSPORIDIA;

EID: 84871859866     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02737-12     Document Type: Article

References (69)

1. Didier ES, Weiss LM. 2006. Microsporidiosis: current status. Curr. Opin. Infect. Dis. 19:485-492.
2. Ortega YR, Sanchez R. 2010. Update on Cyclospora cayetanensis, a foodborne and waterborne parasite. Clin. Microbiol. Rev. 23:218-234.
3. Dowd SE, Gerba CP, Pepper IL. 1998. Confirmation of the humanpathogenic microsporidia Enterocytozoon bieneusi, Encephalitozoon intestinalis, and Vittaforma corneae in water. Appl. Environ. Microbiol. 64: 3332-3335.
4. Dowd SE, John D, Eliopolus J, Gerba CP, Naranjo J, Klein R, Lopez B, de Mejia M, Mendoza CE, Pepper IL. 2003. Confirmed detection of Cyclospora cayetanensis, Encephalitozoon intestinalis and Cryptosporidium parvum in water used for drinking. J. Water Health 1:117-123.
5. Sturbaum GD, Ortega YR, Gilman RH, Sterling CR, Cabrera L, Klein DA. 1998. Detection of Cyclospora cayetanensis in wastewater. Appl. Environ. Microbiol. 64:2284-2286.
6. Cotte L, Rabodonirina M, Chapuis F, Bailly F, Bissuel F, Raynal C, Gelas P, Persat F, Piens MA, Trepo C. 1999. Waterborne outbreak of intestinal microsporidiosis in persons with and without human immunodeficiency virus infection. J. Infect. Dis. 180:2003-2008.
7. Rabold JG, Hoge CW, Shlim DR, Kefford C, Rajah R, Echeverria P. 1994. Cyclospora outbreak associated with chlorinated drinking water. Lancet 344:1360-1361.
8. US Environmental Protection Agency. 2005. Contaminant candidate list 2 and regulatory determinations. US Environmental Protection Agency, Washington, DC. http://water.epa.gov/scitech/drinkingwater/dws/ccl/ccl2.cfm.
9. US Environmental Protection Agency. 2009. Contaminant candidate list 3. US Environmental Protection Agency, Washington, DC. http://water.epa.gov/scitech/drinkingwater/dws/ccl/ccl3.cfm.
10. Izquierdo F, Castro Hermida JA, Fenoy S, Mezo M, Gonzalez-Warleta M, del Aguila C. 2011. Detection of microsporidia in drinking water, wastewater and recreational rivers. Water Res. 45:4837-4843.
11. Magnet A, Galván AL, Fenoy S, Izquierdo F, Rueda C, Fernandez Vadillo C, Pérez-Irezábal J, Bandyopadhyay K, Visvesvara GS, da Silva AJ, del Aguila C. 2012. Molecular characterization of Acanthamoeba isolated in water treatment plants and comparison with clinical isolates. Parasitol. Res. 111:383-392.
12. US Environmental Protection Agency. 2005. Method 1623: Cryptosporidium and Giardia in water by filtration/IMS/FA. US Environmental Protection Agency, Washington, DC. http://water.epa.gov/scitech/methods/cwa/bioindicators/upload/method_1623.pdf.
13. da Silva AJ, Bornay-Llinares FJ, Moura IN, Slemenda SB, Tuttle JL, Pieniazek NJ. 1999. Fast and reliable extraction of protozoan parasite DNA from fecal specimens. Mol. Diagn. 4:57-64.
14. DA Silva AJ, Schwartz DA, Visvesvara GS, de Moura H, Slemenda SB, Pieniazek NJ. 1996. Sensitive PCR diagnosis of Infections by Enterocytozoon bieneusi (microsporidia) using primers based on the region coding for small-subunit rRNA. J. Clin. Microbiol. 34:986-987.
15. DA Silva AJ, Slemenda SB, Visvesvara GS, Schwartz DA, Wilcox CM, Wallace S, Pieniazek NJ. 1997. Detection of Septata intestinalis (Microsporidia) Cali et al. 1993 using polymerase chain reaction primers targeting the small submit subunit ribosomal RNA coding region. Mol. Diagn. 2:47-52.
16. De Groote MA, Visvesvara G, Wilson ML, Pieniazek NJ, Slemenda SB, da Silva AJ, Leitch GJ, Bryan RT, Reves R. 1995. Polymerase chain reaction and culture confirmation of disseminated Encephalitozoon cuniculi in a patient with AIDS: successful therapy with albendazole. J. Infect. Dis. 171:1375-1378.
17. Visvesvara GS, Leitch GJ, DA Silva AJ, Croppo GP, Moura H, Wallace S, Slemenda SB, Schwartz DA, Moss D, Bryan RT, et al. 1994. Polyclonal and monoclonal antibody and PCR-amplified small-subunit rRNA identification of a microsporidian, Encephalitozoon hellem, isolated from an AIDS patient with disseminated infection. J. Clin. Microbiol. 32:2760-2768.
18. Visvesvara GS, Belloso M, Moura H, DA Silva AJ, Moura IN, Leitch GJ, Schwartz DA, Chevez-Barrios P, Wallace S, Pieniazek NJ, Goosey JD. 1999. Isolation of Nosema algerae from the cornea of an immunocompetent patient. J. Eukaryot. Microbiol. 46:10S.
19. Ghosh K, Weiss LM. 2009. Molecular diagnostic tests for microsporidia. Interdiscip. Perspect. Infect. Dis. 2009:926521. doi:10.1155/2009/926521.
20. Galvan AL, Sanchez AM, Valentin MA, Henriques-Gil N, Izquierdo F, Fenoy S, del Aguila C. 2011. First cases of microsporidiosis in transplant recipients in Spain and review of the literature. J. Clin. Microbiol. 49: 1301-1306.
21. Xiao L, Li L, Visvesvara GS, Moura H, Didier ES, Lal AA. 2001. Genotyping Encephalitozoon cuniculi by multilocus analyses of genes with repetitive sequences. J. Clin. Microbiol. 39:2248-2253.
22. Relman DA, Schmidt TM, Gajadhar A, Sogin M, Cross J, Yoder K, Sethabutr O, Echeverria P. 1996. Molecular phylogenetic analysis of Cyclospora, the human intestinal pathogen, suggests that it is closely related to Eimeria species. J. Infect. Dis. 173:440-445.
23. Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41:95-98.
24. Breton J, Bart-Delabesse E, Biligui S, Carbone A, Seiller X, Okome- Nkoumou M, Nzamba C, Kombila M, Accoceberry I, Thellier M. 2007. New highly divergent rRNA sequence among biodiverse genotypes of En-terocytozoon bieneusi strains isolated from humans in Gabon and Cameroon. J. Clin. Microbiol. 45:2580-2589.
25. Chalifoux LV, Carville A, Pauley D, Thompson B, Lackner AA, Mansfield KG. 2000. Enterocytozoon bieneusi as a cause of proliferative serositis in simian immunodeficiency virus-infected immunodeficient macaques (Macaca mulatta). Arch. Pathol. Lab. Med. 124:1480-1484.
26. Henriques-Gil N, Haro M, Izquierdo F, Fenoy S, del Aguila C. 2010. Phylogenetic approach to the variability of the microsporidian Enterocytozoon bieneusi and its implications for inter- and intrahost transmission. Appl. Environ. Microbiol. 76:3333-3342.
27. Santin M, Fayer R. 2009. Enterocytozoon bieneusi genotype nomenclature based on the internal transcribed spacer sequence: a consensus. J. Eukaryot. Microbiol. 56:34-38.
28. Breitenmoser AC, Mathis A, Burgi E, Weber R, Deplazes P. 1999. High prevalence of Enterocytozoon bieneusi in swine with four genotypes that differ from those identified in humans. Parasitology 118:447-453.
29. Dengjel B, Zahler M, Hermanns W, Heinritzi K, Spillmann T, Thomschke A, Loscher T, Gothe R, Rinder H. 2001. Zoonotic potential of Enterocytozoon bieneusi. J. Clin. Microbiol. 39:4495-4499.
30. Liguory O, David F, Sarfati C, Schuitema AR, Hartskeerl RA, Derouin F, Modai J, Molina JM. 1997. Diagnosis of infections caused by Enterocytozoon bieneusi and Encephalitozoon intestinalis using polymerase chain reaction in stool specimens. AIDS 11:723-726.
31. Rinder H, Katzwinkel-Wladarsch S, Loscher T. 1997. Evidence for the existence of genetically distinct strains of Enterocytozoon bieneusi. Parasitol. Res. 83:670-672.
32. Santin M, Trout JM, Vecino JA, Dubey JP, Fayer R. 2006. Cryptosporidium, Giardia and Enterocytozoon bieneusi in cats from Bogota (Colombia) and genotyping of isolates. Vet. Parasitol. 141:334-339.
33. Sharma S, Sachdeva P, Virdi JS. 2003. Emerging water-borne pathogens. Appl. Microbiol. Biotechnol. 61:424-428.
34. del Aguila C, Lopez-Velez R, Fenoy S, Turrientes C, Cobo J, Navajas R, Visvesvara GS, Croppo GP, da Silva AJ, Pieniazek NJ. 1997. Identification of Enterocytozoon bieneusi spores in respiratory samples from an AIDS patient with a 2-year history of intestinal microsporidiosis. J. Clin. Microbiol. 35:1862-1866.
35. del Aguila C, Moura H, Fenoy S, Navajas R, Lopez-Velez R, Li L, Xiao L, Leitch GJ, da Silva AJ, Pieniazek NJ, Lal AA, Visvesvara GS. 2001. In vitro culture, ultrastructure, antigenic, and molecular characterization of Encephalitozoon cuniculi isolated from urine and sputum samples from a Spanish patient with AIDS. J. Clin. Microbiol. 39:1105-1108.
36. Del Aguila C, Navajas R, Gurbindo D, Ramos JT, Mellado MJ, Fenoy S, Munoz Fernandez MA, Subirats M, Ruiz J, Pieniazek NJ. 1997. Microsporidiosis in HIV-positive children in Madrid (Spain). J. Eukaryot. Microbiol. 44:84S- 85S.
37. Lopez-Velez R, Turrientes MC, Garron C, Montilla P, Navajas R, Fenoy S, del Aguila C. 1999. Microsporidiosis in travelers with diarrhea from the tropics. J. Travel Med. 6:223-227.
38. Lores B, Lopez-Miragaya I, Arias C, Fenoy S, Torres J, del Aguila C. 2002. Intestinal microsporidiosis due to Enterocytozoon bieneusi in elderly human immunodeficiency virus-negative patients from Vigo, Spain. Clin. Infect. Dis. 34:918-921.
39. Abreu-Acosta N, Lorenzo-Morales J, Leal-Guio Y, Coronado-Alvarez N, Foronda P, Alcoba-Florez J, Izquierdo F, Batista-Diaz N, Del Aguila C, Valladares B. 2005. Enterocytozoon bieneusi (microsporidia) in clinical samples from immunocompetent individuals in Tenerife, Canary Islands, Spain. Trans. R. Soc. Trop. Med. Hyg. 99:848-855.
40. Hutin YJ, Sombardier MN, Liguory O, Sarfati C, Derouin F, Modai J, Molina JM. 1998. Risk factors for intestinal microsporidiosis in patients with human immunodeficiency virus infection: a case-control study. J. Infect. Dis. 178:904-907.
41. Dascomb K, Frazer T, Clark RA, Kissinger P, Didier E. 2000. Microsporidiosis and HIV. J. Acquir. Immune Defic. Syndr. 24:290-292.
42. Didier ES. 2005. Microsporidiosis: an emerging and opportunistic infection in humans and animals. Acta Trop. 94:61-76.
43. Cheng HW, Lucy FE, Graczyk TK, Broaders MA, Mastitsky SE. 2011. Municipal wastewater treatment plants as removal systems and environmental sources of human-virulent microsporidian spores. Parasitol. Res. 109:595-603.
44. Graczyk TK, Lucy FE, Mashinsky Y, Andrew Thompson RC, Koru O, da Silva AJ. 2009. Human zoonotic enteropathogens in a constructed free-surface flow wetland. Parasitol. Res. 105:423-428.
45. Coupe S, Delabre K, Pouillot R, Houdart S, Santillana-Hayat M, Derouin F. 2006. Detection of Cryptosporidium, Giardia and Enterocytozoon bieneusi in surface water, including recreational areas: a one-year prospective study. FEMS Immunol. Med. Microbiol. 47:351-359.
46. Fournier S, Dubrou S, Liguory O, Gaussin F, Santillana-Hayat M, Sarfati C, Molina JM, Derouin F. 2002. Detection of microsporidia, cryptosporidia and Giardia in swimming pools: a one-year prospective study. FEMS Immunol. Med. Microbiol. 33:209-213.
47. Mathis A, Weber R, Deplazes P. 2005. Zoonotic potential of the microsporidia. Clin. Microbiol. Rev. 18:423-445.
48. Haro M, Izquierdo F, Henriques-Gil N, Andres I, Alonso F, Fenoy S, del Aguila C. 2005. First detection and genotyping of human-associated microsporidia in pigeons from urban parks. Appl. Environ. Microbiol. 71:3153-3157.
49. Slodkowicz-Kowalska A, Graczyk TK, Tamang L, Jedrzejewski S, Nowosad A, Zduniak P, Solarczyk P, Girouard AS, Majewska AC. 2006. Microsporidian species known to infect humans are present in aquatic birds: implications for transmission via water? Appl. Environ. Microbiol. 72:4540-4544.
50. Sulaiman IM, Fayer R, Lal AA, Trout JM, Schaefer FW, III, Xiao L. 2003. Molecular characterization of microsporidia indicates that wild mammals harbor host-adapted Enterocytozoon spp. as well as humanpathogenic Enterocytozoon bieneusi. Appl. Environ. Microbiol. 69:4495-4501.
51. Sparfel JM, Sarfati C, Liguory O, Caroff B, Dumoutier N, Gueglio B, Billaud E, Raffi F, Molina JM, Miegeville M, Derouin F. 1997. Detection of microsporidia and identification of Enterocytozoon bieneusi in surface water by filtration followed by specific PCR. J. Eukaryot. Microbiol. 44: 78S.
52. Visvesvara GS, Moura H, Leitch GJ, Schwartz DA, Xiao LX. 2005. Public health importance of Brachiola algerae (Microsporidia)-an emerging pathogen of humans. Folia Parasitol. (Praha) 52:83-94.
53. Didier ES, Stovall ME, Green LC, Brindley PJ, Sestak K, Didier PJ. 2004. Epidemiology of microsporidiosis: sources and modes of transmission. Vet. Parasitol. 126:145-166.
54. Thellier M, Breton J. 2008. Enterocytozoon bieneusi in human and animals, focus on laboratory identification and molecular epidemiology. Parasite 15:349-358.
55. Sherchand JB, Cross JH, Jimba M, Sherchand S, Shrestha MP. 1999. Study of Cyclospora cayetanensis in health care facilities, sewage water and green leafy vegetables in Nepal. Southeast Asian J. Trop. Med. Public Health 30:58-63.
56. Madico G, McDonald J, Gilman RH, Cabrera L, Sterling CR. 1997. Epidemiology and treatment of Cyclospora cayetanensis infection in Peruvian children. Clin. Infect. Dis. 24:977-981.
57. Tram NT, Hoang LM, Cam PD, Chung PT, Fyfe MW, Isaac-Renton JL, Ong CS. 2008. Cyclospora spp. in herbs and water samples collected from markets and farms in Hanoi, Vietnam. Trop. Med. Int. Health 13:1415-1420.
58. Vuong TA, Nguyen TT, Klank LT, Phung DC, Dalsgaard A. 2007. Faecal and protozoan parasite contamination of water spinach (Ipomoea aquatica) cultivated in urban wastewater in Phnom Penh, Cambodia. Trop. Med. Int. Health 12(Suppl 2):73-81.
59. Lopez AS, Bendik JM, Alliance JY, Roberts JM, da Silva AJ, Moura IN, Arrowood MJ, Eberhard ML, Herwaldt BL. 2003. Epidemiology of Cyclospora cayetanensis and other intestinal parasites in a community in Haiti. J. Clin. Microbiol. 41:2047-2054.
60. Miegeville M, Koubi V, Dan LC, Barbier JP, Cam PD. 2003. Cyclospora cayetanensis presence in aquatic surroundings in Hanoi (Vietnam). Environmental study (well water, lakes and rivers). Bull. Soc. Pathol. Exot. 96:149-152.
61. Bern C, Hernandez B, Lopez MB, Arrowood MJ, de Mejia MA, de Merida AM, Hightower AW, Venczel L, Herwaldt BL, Klein RE. 1999. Epidemiologic studies of Cyclospora cayetanensis in Guatemala. Emerg. Infect. Dis. 5:766-774.
62. Fryauff DJ, Krippner R, Prodjodipuro P, Ewald C, Kawengian S, Pegelow K, Yun T, von Heydwolff-Wehnert C, Oyofo B, Gross R. 1999. Cyclospora cayetanensis among expatriate and indigenous populations of West Java, Indonesia. Emerg. Infect. Dis. 5:585-588.
63. Gascon J, Alvarez M, Eugenia Valls M, Maria Bordas J, Teresa Jimenez De Anta M, Corachan M. 2001. Cyclosporiasis: a clinical and epidemiological study in travellers with imported Cyclospora cayetanensis infection. Med. Clin. (Barc.) 116:461-464. (In Spanish.)
64. el-Karamany EM, Zaher TI, el-Bahnasawy MM. 2005. Role of water inthe transmission of cyclosporiarsis in Sharkia Governorate, Egypt. J. Egypt Soc. Parasitol. 35:953-962.
65. Elshazly AM, Elsheikha HM, Soltan DM, Mohammad KA, Morsy TA. 2007. Protozoal pollution of surface water sources in Dakahlia Governorate, Egypt. J. Egypt Soc. Parasitol. 37:51-64.
66. Cordon GP, Prados AH, Romero D, Moreno MS, Pontes A, Osuna A, Rosales MJ. 2009. Intestinal and haematic parasitism in the birds of the Almunecar (Granada, Spain) ornithological garden. Vet. Parasitol. 165: 361-366.
67. Garcia-Lopez HL, Rodriguez-Tovar LE, Medina-De la Garza CE. 1996. Identification of Cyclospora in poultry. Emerg. Infect. Dis. 2:356-357.
68. Li G, Xiao S, Zhou R, Li W, Wadeh H. 2007. Molecular characterization of Cyclospora-like organism from dairy cattle. Parasitol. Res. 100:955-961.
69. Harrington G, Xagoraraki I, Assavasilavasukul P, Standridge J. 2003. Effect of filtration conditions on removal of emerging waterborne pathogens. J. Am Water Works Assoc. 95:95-104